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Diverse Picornaviruses Prevalent Among Free-Living and Laboratory

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Diverse Picornaviruses Prevalent Among Free-Living and Laboratory The original published PDF available in this website: https://www.sciencedirect.com/science/article/pii/S1567134819302060?via%3Dihub Diverse picornaviruses are prevalent among free-living and laboratory rats (Rattus norvegicus) in Hungary and can cause disseminated infections Ákos Borosa, Katalin Orlovácza, Péter Pankovicsa, Sándor Szekeresb, Gábor Földvárib,c, Elizabeth Fahsbenderd, Eric Delwartd,e, Gábor Reutera*, a Department of Medical Microbiology and Immunology, Medical School, University of Pécs Pécs, Hungary b Department of Parasitology and Zoology, University of Veterinary Medicine, Budapest, Hungary c Evolutionary Systems Research Group MTA Centre for Ecological Research, Tihany, Hungary d Vitalant Research Institute, San Francisco, CA, USA e University of California, San Francisco, CA, USA Running title: Prevalent picornaviruses in wild and laboratory rats *Address for correspondence: Dr Gábor Reuter Department of Medical Microbiology and Immunology University of Pécs H-7624, Szigeti út 12., Pécs, Hungary Telephone: +36 (72) 536-252 1 E-mail: [email protected] 2 Abstract In this study, the full length genomes of three phylogenetically distant picornaviruses (family Picornaviridae) belonging to the genus Rosavirus (rat08/rRoB/HUN, MN116648), Kobuvirus (rat08/rAiA/HUN, MN116647), and Cardiovirus (rat08/rCaB/HUN, MN116646) were obtained from a single faecal sample of a free-living Norway rat (Rattus norvegicus) in Hungary using viral metagenomics and RT-PCR/Sanger sequencing. The acquired complete genomes were in silico analyzed in detail revealing the presence of a second minor open reading frame encoding an alternative Leader peptide (L*) in rat08/rCaB/HUN and a ca. 222 nt-long sequence repeat with compact secondary RNA structure in the 3’ UTR of rat08/rRoB/HUN. The studied rat picornaviruses were frequently detectable by RT-PCR with relatively high viral loads ranged between 8.99E+02 and 1.29E+06 copies/ml in rat faecal samples collected from five geographically distant locations throughout Hungary. The VP1 sequence-based phylogenetic analyses show the presence of multiple, mostly location-specific lineages for all three picornaviruses. Rat rosavirus and rat cardiovirus were identified in spleen while rat cardiovirus was also detected in liver, muscle and kidney samples with variable copy numbers (6.42E+01 − 1.90E+05 copies/µg total RNA) suggesting extra-intestinal dissemination. Both viruses were also prevalent (70.0% and 18.2%) among two populations of laboratory rats (“Wistar-type” and “hooded-type”) held in different, isolated laboratory animal units. Keywords rat, picornavirus, extraintestinal, rosavirus, kobuvirus, cardiovirus, 3 1. Introduction Members of family Picornaviridae have positive sense, single-stranded RNA genomes ranging between 7.2 and 9.7 kb (Palmenberg et al., 2010). Picornaviruses (PVs) generally have a single major open reading frame (ORF) flanked by 5’ and 3’ untranslated regions (UTRs), although there are certain PVs such as TO subtypes of Theiler's encephalomyelitis virus (TMEV) of genus Cardiovirus where an additional minor ORF encodes an alternative Leader (L) peptide was also present (Palmenberg et al., 2010; Takano-Maruyama et al., 2006). The genome layouts of PVs include the 5’UTR- ORF: [L (not always present)-VP0 (could be cleaved into VP4 and VP2)-VP3-VP1-2A-2B-2C-3A-3B-3C-3D]-3’UTR-polyA-tail (Palmenberg et al., 2010). The highly structured 5’ UTRs contain predominantly one of the five types of internal ribosomal entry sites (IRES) while the 3’UTRs could contain conserved RNA motifs like s2m, “barbell-like” structures or multiple repeated sequences (Palmenberg et al., 2010; Kofstad & Jonassen, 2011; Boros et al., 2014). The family Picornaviridae currently consists of 110 species grouped into 47 genera and several unassigned PVs (Zell et al., 2017; www.picornaviridae.com). Due to the species richness (ca. 2200 known rodent species) and close contact to humans rodents have one of the highest numbers of discovered viruses including PVs (Chen et al., 2017). The majority of the currently known rodent PVs belong to 11 of the 47 picornavirus genera including Cardiovirus, Kobuvirus and the recently established Rosavirus (Chen et al., 2017; www.picornaviridae.com). The novel genus Rosavirus currently consist of three species (Rosavirus A-C) mainly of rat and mouse viruses (Phan et al., 2011; Lau et al., 2016). Novel Rosavirus A2 (species Rosavirus A) sequences were also identified from pediatric diarrheic faecal specimens in Gambia (Lim et al., 2014). The genus Cardiovirus currently contains several well-known PVs including the Encephalomyocarditis virus (EMCV, Cardiovirus A), which can infect a wide range of animals, the TMEV of mice, the Vilyuisk human encephalomyelitis virus (VHEV) 4 and human Saffold viruses of species Cardiovirus B, the baboon cardioviruses of Cardiovirus C and several currently unpublished cardiovirus sequences from different rat species (Zell et al., 2017; www.picornaviridae.com). From the six official kobuvirus species (Aichivirus A-F) only the Aichivirus A contains rodent viruses (Murine kobuvirus-1, MuKV-1) together with different genotypes identified from humans, cats, dogs and birds as well (Zell et al., 2017). Currently, only partial VP1 sequences and a single unpublished complete genome of MuKV- 1-related rat kobuvirus (rat/Wencheng-Rt386-2/China/2012, MF352432) has been known (Firth et al., 2014; www.picornaviridae.com). With a few exceptions (the pathogenesis of Rosavirus C or the genomic diversity of rodent kobuviruses), the prevalence, genomic diversity and extraintestinal presence or viral load of these viruses in rats are not investigated before (Lau et al., 2016; Lu et al., 2018). Rodents, including different types of rats such as black rat (Rattus rattus) or brown rat/Norway rat (Rattus norvegicus), may serve as potential reservoirs of various known and novel pathogens including (picorna)viruses and due to the overlapping habitats and frequent interactions with humans these animals could be major sources of zoonotic infections (Chen et al., 2017; Strand & Lundkvist, 2019). Furthermore, besides the free-living rodent populations, various types of Norway rats (e.g. “Wistar-type” or “hooded-type”) are extensively used as experimental animal models for diverse scientific research projects (Baker et al., 2013). Although separate populations of these animals are usually bred and held in special laboratory animal facilities/units with high hygienic standards little information is available about the viruses circulating in such experimental animal populations. In this study, the complete genomes of three phylogenetically distant PVs belonging to the genus Cardiovirus, Kobuvirus and Aichivirus were characterized by viral metagenomic and RT-PCR from a single faecal sample of a free-living Norway rat in Hungary and analyzed in detail. The prevalence, genomic diversity of these PVs and virus RNA detection (RT- 5 PCR/qPCR) from extra-intestinal tissues (including absolute copy numbers) of these PVs were also investigated. The study viruses were prevalent among free-living animals originated from geographically distant locations in Hungary and in a subset of laboratory rats (“Wistar- type” and “hooded-type”) held in isolated laboratory animal units. 2. Materials and methods 2.1.Background data of the sampled animals Total of 10 (N=3 juvenile, N=7 adult, animal IDs: rat-01 – rat-10) free-living Norway rats (Rattus norvegicus) with unknown health status were trapped by mechanic rat-traps from backyards of small livestock farms from five different geographical locations in Hungary between July 2017 and April 2018 (Fig. 1A). Faecal samples from 9 of the 10 trapped animals as well as various tissue specimens from all carcasses were collected for further analyses (Table 1). An additional 21 faecal samples (N=10 adult “Wistar-type”, N= 11 “hooded-type”) were also collected from Norway rats bred and held in two separate laboratory animal units in May 2019 in University of Pécs, Pécs, Hungary (Fig.1A). All of the apparently healthy sampled animals were held in separate cages. All faecal and tissue specimens were stored in -80oC until further processing. 2.2.Viral metagenomics, next-generation sequencing and bioinformatics analyses A single pooled specimen which contained four randomly selected faecal samples of free- living Norway rats (rat-01; -04; -08; -09) collected from geographically distant locations in Hungary (Budapest, Hajdúböszörmény, Rácalmás and Zimány) (Fig. 1A) were subjected to viral metagenomic analysis using random (RT-)PCR amplification of viral-particle protected nucleic acids as previously described (Phan et al. 2013b). Briefly, 200 ml of the supernatant of centrifuged (15,000g for 10 min) faecal suspension was filtered through a 0.45-mm filter 6 (Millipore) and then treated with a mixture of DNases (Turbo DNase from Ambion, Baseline- ZERO from Epicentre, and Benzonase from Novagen) and RNase (Fermentas) to digest unprotected nucleic acids. Viral cDNA library was constructed by ScriptSeqTM v2 RNA-Seq Library Preparation Kit (Epicentre) and sequenced using the MiSeq Illumina platform. The generated sequence reads (singletons) were assembled to contigs and sequences (reads and contigs) longer than 100-bp were compared to the protein database of GenBank using BLASTx. The Expected value (E) cut-off was set up to 10-5 for the categorization of the reads. Only sequences with better matches to known viruses were analysed further. 2.3.Genome acquisition
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